Abstract
A rapid decline in egg production of laying hens begins after 480 d of age. Such a rapid decrease results predominantly from the ovarian aging, accompanied by endocrine changes, decreased yolk synthesis and accumulation, and the reduction in follicles selected into the preovulatory hierarchy. In this study, hens at 90, 150, 280, and 580 d old (D90, D150, D280, and D580, respectively) were compared for yolk precursor formation in the liver to elucidate effects of aging on laying performance. The results showed that liver lipid synthesis increased remarkably in hens from D90 to D150, but decreased sharply at D580 as indicated by the changes in triglyceride (TG) levels. This result was consistent with the age-related changes of the laying performance. The levels of liver antioxidants and total antioxidant capacity decreased significantly in D580 hens and the methane dicarboxylic aldehyde in D580 hens was much higher than that at other stages. The serum 17β-estradiol level increased from D90 to D280, but decreased at D580 ({itP}<0.05). The expression of estrogen receptor α and β mRNAs in the liver displayed similar changes to the serum 17β-estradiol in D580 hens. Expressions of the genes related to yolk precursor formation and enzymes responsible for fat acid synthesis were all decreased in D580 hens. These results indicated that decreased yolk precursor formation in the liver of the aged hens resulted from concomitant decreases of serum 17β-estradiol level, transcription levels of estrogen receptors and critical genes involved in yolk precursor synthesis, and liver antioxidant status.
中文概要
目的
比较不同日龄蛋鸡血清雌激素的水平、肝脏雌激 素受体基因和卵黄前体物生成相关基因表达量、 “肝脏-血液-卵巢轴”中甘油三酯和胆固醇的含 量和肝脏抗氧化能力的动态变化,揭示蛋鸡卵黄 前体物生成随着年龄增长的变化规律。
创新点
首次发现在蛋鸡衰老过程中雌激素作用衰退以及 肝脏抗氧化能力降低致使肝脏中卵黄前体物合 成下降,最终导致蛋鸡的产蛋性能下降。
方法
取90、150、280 和580 日龄蛋鸡各10 只,检测 血清中雌激素水平、肝脏雌激素受体基因表达水 平、肝脏中卵黄前体物质合成和脂质代谢相关基 因表达水平、“肝脏-血液-卵巢轴”中甘油三酯 和胆固醇的含量及肝脏抗氧化能力,揭示蛋鸡卵 黄前体物生成在衰老过程中的变化规律。
结论
在蛋鸡衰老过程中,血清雌激素水平、肝脏雌激 素受体基因和卵黄前体物质合成相关基因表达 量降低,肝脏抗氧化能力降低,引起肝脏合成甘 油三酯的能力下降,最终导致卵黄前体物质合成 能力降低。
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bahr JM, Johnson AL, 1984. Regulation of the follicular hierarchy and ovulation. J Exp Zool, 232(3):495–500. https://doi.org/10.1002/jez.1402320316
Bai J, Greene E, Li W, et al., 2015. Branched-chain amino acids modulate the expression of hepatic fatty acid metabolism-related genes in female broiler chickens. Mol Nutr Food Res, 59(6):1171–1181. https://doi.org/10.1002/mnfr.201400918
Ben-Meir A, Burstein E, Borrego-Alvarez A, et al., 2015. Coenzyme Q10 restores oocyte mitochondrial function and fertility during reproductive aging. Aging Cell, 14(5): 887–895. https://doi.org/10.1111/acel.12368
Buyuk E, Nejat E, Neal-Perry G, 2010. Determinants of female reproductive senescence: differential roles for the ovary and the neuroendocrine axis. Semin Reprod Med, 28(5): 370–379. https://doi.org/10.1055/s-0030-1262896 Claire
D'Andre H, Paul W, Shen X, et al., 2013. Identification and characterization of genes that control fat deposition in chickens. J Anim Sci Biotechnol, 4(1):43–58. https://doi.org/10.1186/2049-1891-4-43
Cohen A, Smith Y, 2014. Estrogen regulation of microRNAs, target genes, and microRNA expression associated with vitellogenesis in the zebrafish. Zebrafish, 11(5):462–478. https://doi.org/10.1089/zeb.2013.0873
Ge C, Yu M, Zhang C, 2012. G protein-coupled receptor 30 mediates estrogen-induced proliferation of primordial germ cells via EGFR/Akt/β-catenin signaling pathway. Endocrinology, 153(7):3504–3516. https://doi.org/10.1210/en.2012-1200
Hall JM, Couse JF, Korach KS, 2001. The multifaceted mechanisms of estradiol and estrogen receptor signaling. J Biol Chem, 276(40):36869–36872. https://doi.org/10.1074/jbc.R100029200
Hess RA, Fernandes SAF, Gomes GRO, et al., 2011. Estrogen and its receptors in efferent ductules and epididymis. J Androl, 32(6):600–613. https://doi.org/10.2164/jandrol.110.012872
Hoare M, Das T, Alexander G, 2010. Ageing, telomeres, senescence, and liver injury. J Hepatol, 53(5):950–961. https://doi.org/10.1016/j.jhep.2010.06.009
Ishii M, Yamauchi T, Matsumoto K, et al., 2012. Maternal age and reproductive function in female Sprague-Dawley rats. J Toxicol Sci, 37(3):631–638. https://doi.org/10.2131/jts.37.631
Johnson A, 2015. Reproduction in the female. In: Scanes CG (Ed.), Sturkie’s Avian Physiology, 6th Ed. Academic Press, London, p.653–654.
Joyner CJ, Peddie MJ, Taylor TG, 1987. The effect of age on egg production in the domestic hen. Gen Comp Endocrinol, 65(3):331–336. https://doi.org/10.1016/0016-6480(87)90117-1
Khalil HA, Hanafy AM, Saleh SY, et al., 2009. Comparative changes in the serum concentrations of inhibin-B, prolactin, gonadotropins and steroid hormones at different reproductive states in domestic Turkey hens. J Reprod Dev, 55(5):523–528. https://doi.org/10.1262/jrd.20137
Kim CH, Song JH, Lee JC, et al., 2014. Age-related changes in egg quality of Hy-Line brown hens. Int J Poult Sci, 13(9):510–514. https://doi.org/10.3923/ijps.2014.510.514
Leaños-Castañeda O, van der Kraak G, 2007. Functional characterization of estrogen receptor subtypes, ERα and ERβ, mediating vitellogenin production in the liver of rainbow trout. Toxicol Appl Pharmacol, 224(2):116–125. https://doi.org/10.1016/j.taap.2007.06.017
Li H, Wang T, Xu C, et al., 2015. Transcriptome profile of liver at different physiological stages reveals potential mode for lipid metabolism in laying hens. BMC Genomics, 16:763–775. https://doi.org/10.1186/s12864-015-1943-0
Li J, Leghari IH, He B, et al., 2014. Estrogen stimulates expression of chicken hepatic vitellogenin II and very lowdensity apolipoprotein II through ER-α. Theriogenology, 82(3):517–524. https://doi.org/10.1016/j.theriogenology.2014.05.003
Lillpers K, Wilhelmson M, 1993. Age-dependent changes in oviposition pattern and egg production traits in the domestic hen. Poult Sci, 72(11):2005–2011. https://doi.org/10.3382/ps.0722005
Nagahama Y, 1994. Endocrine regulation of gametogenesis in fish. Int J Dev Biol, 38(2):217–229.
Okudan N, Belviranli M, 2016. Effects of exercise training on hepatic oxidative stress and antioxidant status in aged rats. Arch Physiol Biochem, 122(4):180–185. https://doi.org/10.1080/13813455.2016.1199574
Palmer SS, Bahr JM, 1992. Follicle stimulating hormone increases serum oestradiol-17β concentrations, number of growing follicles and yolk deposition in aging hens (Gallus gallus domesticus) with decreased egg production. Br Poult Sci, 33(2):403–414. https://doi.org/10.1080/00071669208417478
Ratna WN, Bhatt VD, Chaudhary K, et al., 2016. Estrogenresponsive genes encoding egg yolk proteins vitellogenin and apolipoprotein II in chicken are differentially regulated by selective estrogen receptor modulators. Theriogenology, 85(3):376–383. https://doi.org/10.1016/j.theriogenology.2015.08.015
Reddy IJ, David CG, Sarma PV, et al., 2002. The possible role of prolactin in laying performance and steroid hormone secretion in domestic hen (Gallus domesticus). Gen Comp Endocrinol, 127(3):249–255. https://doi.org/10.1016/S0016-6480(02)00034-5
Subramanian MV, James TJ, 2010. Age-related protective effect of deprenyl on changes in the levels of diagnostic marker enzymes and antioxidant defense enzymes activities in cerebellar tissue in Wistar rats. Cell Stress Chaperon, 15(5):743–751. https://doi.org/10.1007/s12192-010-0177-y
Tong L, Chuang CC, Wu S, et al., 2015. Reactive oxygen species in redox cancer therapy. Cancer Lett, 367(1): 18–25. https://doi.org/10.1016/j.canlet.2015.07.008
Verderame M, Limatola E, 2010. Molecular identification of estrogen receptors (ERα and ERβ) and their differential expression during VTG synthesis in the liver of lizard Podarcis sicula. Gen Comp Endocrinol, 168(2):231–238. https://doi.org/10.1016/j.ygcen.2010.04.014
Yilmaz O, Prat F, Ibañez AJ, et al., 2015. Estrogen-induced yolk precursors in European sea bass, Dicentrarchus labrax: status and perspectives on multiplicity and functioning of vitellogenins. Gen Comp Endocrinol, 221: 16–22. https://doi.org/10.1016/j.ygcen.2015.01.018
Zakaria AH, Miyaki T, Imai K, 1983. The effect of aging on the ovarian follicular growth in laying hens. Poult Sci, 62(4):670–674. https://doi.org/10.3382/ps.0620670
Zhang R, Hu Y, Wang H, et al., 2016. Molecular cloning, characterization, tissue distribution and mRNA expression changes during the hibernation and reproductive periods of estrogen receptor alpha (ESR1) in Chinese alligator, Alligator sinensis. Comp Biochem Physiol B, 200: 28–35. https://doi.org/10.1016/j.cbpb.2016.05.001
Acknowledgements
We sincerely thank Chang-quan GUO, Guang LIU, and Rong-xia LI (College of Animal Sciences, Zhejiang University, Hangzhou, China) for their help in the experiments.
Author information
Authors and Affiliations
Corresponding author
Additional information
Project supported by the National Natural Science Foundation of China (Nos. 31472160 and 31272525)
Rights and permissions
About this article
Cite this article
Liu, Xt., Lin, X., Mi, Yl. et al. Age-related changes of yolk precursor formation in the liver of laying hens. J. Zhejiang Univ. Sci. B 19, 390–399 (2018). https://doi.org/10.1631/jzus.B1700054
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1631/jzus.B1700054